Abstract
Fluoride is widely distributed in the environment and has been associated with the development of different health hazards in animals and humans. Argan oil (AO) is a natural vegetable oil with various beneficial pharmacological effects. This study was designed to investigate the potential protective effect of AO supplementation as pre-treatment or co-treatment on sodium fluoride (NaF)–induced nephrotoxicity in rats. Male Sprague Dawley rats (n = 50) were randomly assigned to one of five equal groups: control group, AO-treated group (6 ml/kg b.wt.), NaF-treated group (20 mg/kg b.wt.), pre-treated group, and co-treated group. All rats were daily administered by oral gavage for duration of 30 days. The results showed that AO administration significantly improved renal function and antioxidant status and decreased the lipid peroxidation in NaF-treated rats. Additionally, AO normalized the renal levels of inflammatory markers and mRNA expression level of the intermediate filament protein genes, indicating NaF-induced podocyte damage was ameliorated. Histopathological evaluation of the kidney confirmed the before mentioned biochemical results. AO counteracted the nephrotoxic effects of NaF in rats particularly at co-exposure. These results concluded that AO administration exhibited a significant nephroprotective effect against renal injury induced by NaF in rats.
Similar content being viewed by others
References
Agency for Toxic Substances and Disease Registry (ATSDR) (2003) Toxicological profile for fluorides, hydrogen fluoride, and fluorine. US Department of Health and Human Services, Atlanta, US
Alhusaini AM, Faddah LM, El Orabi NF, Hasan IH (2018) Role of some natural antioxidants in the modulation of some proteins expressions against sodium fluoride-induced renal injury. Biomed Res Int 2018:5614803
Arisha AH, Moustafa A (2019) Potential inhibitory effect of swimming exercise on the Kisspeptin-GnRH signaling pathway in male rats. Theriogenology 133:87–96
Arisha AH, Ahmed MM, Kamel MA, Attia YA, Hussein MMA (2019) Morin ameliorates the testicular apoptosis, oxidative stress, and impact on blood-testis barrier induced by photo-extracellularly synthesized silver nanoparticles. Environ Sci Pollut Res 26:28749–28762
Awad A, Khalil SR, Farag MR, Nassan MA (2018) Differential susceptibility of kidneys and livers to proliferative processes and transcriptional level of the genes encoding desmin, vimentin, connexin 43, and nestin in rats exposed to furan. Ecotoxicol Environ Saf 162:235–244
Aydin B (2017) Effects of argan oil on the mitochondrial function, antioxidant system and the activity of NADPH- generating enzymes in acrylamide treated rat brain. Biomed Pharmacother 87:476–481
Bakour M, Soulo N, Hammas N, Fatemi HE, Aboulghazi A, Taroq A, Abdellaoui A, Al-Waili N, Lyoussi B (2018) The antioxidant content and protective effect of argan oil and Syzygium aromaticum essential oil in hydrogen peroxide-induced biochemical and histological changes. Int J Mol Sci 19:610
Bancroft JD, Gamble M (2008) Theory and practice of histological techniques. Philadelphia /Elsevier, Churchill Livingstone, London - New York
Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888
Bravo J, Quiroz Y, Pons H, Parra G, Herrera-Acosta J, Johnson RJ, Rodriguez-Iturbe B (2003) Vimentin and heat shock protein expression are induced in the kidney by angiotensin and by nitric oxide inhibition. Kidney Int Suppl: S46-51
Charrouf Z, Guillaume D (2008) Argan oil: occurrence, composition and impact on human health. Eur J Lipid Sci Technol 110:632–636
Coimbra TM, Janssen U, Gröne HJ, Ostendorf T, Kunter U, Schmidt H, Brabant G, Floege J (2000) Early events leading to renal injury in obese Zucker (fatty) rats with type II diabetes. Kidney Int 57:167–182
DePianto D, Coulombe PA (2004) Intermediate filaments and tissue repair. Exp Cell Res 301:68–76
Deshmane SL, Kremlev S, Amini S, Sawaya BE (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interf Cytokine Res 29:313–326
El Abbassi A, Khalid N, Zbakh H, Ahmad A (2014) Physicochemical characteristics, nutritional properties, and health benefits of argan oil: a review. Crit Rev Food Sci Nutr 54:1401–1414
El Kamouni S, El Kebbaj R, Andreoletti P, El Ktaibi A, Rharrassi I, Essamadi A, El Kebbaj MS, Mandard S, Latruffe N, Vamecq J, Nasser B, Cherkaoui-Malki M (2017) Protective effect of argan and olive oils against lps-induced oxidative stress and inflammation in mice livers. Int J Mol Sci 18:2181
El Midaoui A, Haddad Y, Filali-Zegzouti Y, Couture R (2017) Argan oil as an effective nutri-therapeutic agent in metabolic syndrome: a preclinical study. Int J Mol Sci 18:2492
Ghosh D, Das Sarkar S, Maiti R, Jana D, Das UB (2002) Testicular toxicity in sodium fluoride treated rats: association with oxidative stress. Reprod Toxicol 16:385–390
Gross RT, Bracci R, Rudolph N, Schroeder E, Kochen JA (1967) Hydrogen peroxide toxicity and detoxification in the erythrocytes of newborn infants. Blood 29:481–493
Haimeur A, Messaouri H, Ulmann L, Mimouni V, Masrar A, Chraibi A, Tremblin G, Meskini N (2013) Argan oil prevents prothrombotic complications by lowering lipid levels and platelet aggregation, enhancing oxidative status in dyslipidemic patients from the area of Rabat (Morocco). Lipids Health Dis 12:107
Haller H, Bertram A, Nadrowitz F, Menne J (2016) Monocyte chemoattractant protein-1 and the kidney. Curr Opin Nephrol Hypertens 25:42–49
Kanagaraj VV, Panneerselvam L, Govindarajan V, Ameeramja J, Perumal E (2015) Caffeic acid, a phyto polyphenol mitigates fluoride induced hepatotoxicity in rats: a possible mechanism. Biofactors 41:90–100
Kerjaschki D (1994) Dysfunctions of cell biological mechanisms of visceral epithelial cell (podocytes) in glomerular diseases. Kidney Int 45:300–313
Khalil SR, Mohammed AT, Abd El-Fattah AH, Zaglool AW (2018) Intermediate filament protein expression pattern and inflammatory response changes in kidneys of rats receiving doxorubicin chemotherapy and quercetin. Toxicol Lett 288:89–98
Khallouki F, Younos C, Soulimani R, Oster T, Charrouf Z, Spiegelhalder B, Bartsch H, Owen RW (2003) Consumption of argan oil (Morocco) with its unique profile of fatty acids, tocopherols, squalene, sterols and phenolic compounds should confer valuable cancer chemopreventive effects. Eur J Cancer Prev 12:67–75
Khamis T, Abdelalim AF, Abdallah SH, Saeed AA, Edress NM, Arisha AH (2020) Early intervention with breast milk mesenchymal stem cells attenuates the development of diabetic-induced testicular dysfunction via hypothalamic Kisspeptin/Kiss1r-GnRH/GnIH system in male rats. Biochim Biophys Acta Mol basis Dis 1866:165577
Kono K, Kamijo Y, Hora K, Takahashi K, Higuchi M, Kiyosawa K, Shigematsu H, Gonzalez FJ, Aoyama T (2009) PPAR {alpha} attenuates the proinflammatory response in activated mesangial cells. Am J Physiol Renal Physiol 296:F328–F336
Koracevic D, Koracevic G, Djordjevic V, Andrejevic S, Cosic V (2001) Method for the measurement of antioxidant activity in human fluids. J Clin Pathol 54:356–361
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Lizard G, Filali-Zegzouti Y, Midaoui AE (2017) Benefits of argan oil on human health-May 4-6 2017, Errachidia, Morocco. Int J Mol Sci 18:1383
Luo Q, Cui H, Deng H, Kuang P, Liu H, Lu Y, Fang J, Zuo Z, Deng J, Li Y, Wang X, Zhao L (2017) Sodium fluoride induces renal inflammatory responses by activating NF-κB signaling pathway and reducing anti-inflammatory cytokine expression in mice. Oncotarget 8:80192–80207
Mansour HH, Tawfik SS (2012) Efficacy of lycopene against fluoride toxicity in rats. Pharm Biol 50:707–711
Mesram N, Nagapuri K, Banala RR, Nalagoni CR, Karnati PR (2017) Quercetin treatment against NaF induced oxidative stress related neuronal and learning changes in developing rats. J King Saud Univ Sci 29:221–229
Michalczyk K, Ziman M (2005) Nestin structure and predicted function in cellular cytoskeletal organisation. Histol Histopathol 20:665–671
Miltonprabu S, Thangapandiyan S (2015) Epigallocatechin gallate potentially attenuates fluoride induced oxidative stress mediated cardiotoxicity and dyslipidemia in rats. J Trace Elem Med Biol 29:321–335
Mohammed AT, Mohamed AA, Ali H (2017) Pulmonary apoptotic and oxidative damaging effects of Triclosan alone or in combination with fluoride in Sprague Dawley rats. Acta Histochem 119:357–363
Nabavi SM, Nabavi SF, Habtemariam S, Moghaddam AH, Latifi AM (2012) Ameliorative effects of quercetin on sodium fluoride-induced oxidative stress in rat's kidney. Ren Fail 34:901–906
Nabavi SM, Habtemariam S, Nabavi SF, Sureda A, Daglia M, Moghaddam AH, Amani MA (2013) Protective effect of gallic acid isolated from Peltiphyllum peltatum against sodium fluoride-induced oxidative stress in rat's kidney. Mol Cell Biochem 372:233–239
National Research Council (NRC) (2006) Fluoride in drinking water: a scientific review of EPAʼs standards. The National Academies Press, Washington, DC
Necib Y, Bahi A, Zerizer S (2013) Amelioration of mercuric chloride toxicity on rat liver with Argan oil and sodium selenite supplements. Int J Pharm Bio Sci 4:839–849
Nishikimi M, Roa NA, Yogi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulphate and molecular oxygen. Biochem Bioph Res Common 46:849–854
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358
Sekeroglu ZA, Aydin B, Sekeroglu V (2017) Argan oil reduces oxidative stress, genetic damage and emperipolesis in rats treated with acrylamide. Biomed Pharmacother 94:873–879
Shanmugam T, Abdulla S, Yakulasamy V, Selvaraj M, Mathan R (2018) A mechanism underlying the neurotoxicity induced by sodium fluoride and its reversal by epigallocatechin gallate in the rat hippocampus: involvement of NrF2/Keap-1 signaling pathway. J Basic Appl Zool 79:17
Shanthakumari D, Srinivasalu S, Subramanian S (2004) Effect of fluoride intoxication on lipidperoxidation and antioxidant status in experimental rats. Toxicology 204:219–228
Shulman JD, Wells LM (1997) Acute fluoride toxicity from ingesting home-use dental products in children, birth to 6 years of age. J Public Health Dent 57:150–158
Song C, Fu B, Zhang J, Zhao J, Yuan M, Peng W, Zhang Y, Wu H (2017) Sodium fluoride induces nephrotoxicity via oxidative stress-regulated mitochondrial SIRT3 signaling pathway. Sci Rep 7:672
Thangapandiyan S, Miltonprabu S (2014) Epigallocatechin gallate supplementation protects against renal injury induced by fluoride intoxication in rats: role of Nrf2/HO-1 signaling. Toxicol Rep 1:12–30
Tian X, Xie J, Chen X, Dong N, Feng J, Gao Y, Tian F, Zhang W, Qiu Y, Niu R, Ren X, Yan X (2020) Deregulation of autophagy is involved in nephrotoxicity of arsenite and fluoride exposure during gestation to puberty in rat offspring. Arch Toxicol 94:749–760
Vani ML, Reddy KP (2000) Effects of fluoride accumulation on some enzymes of brain and gastrocnemius muscle of mice. Fluoride 33:17–26
Vansthertem D, Gossiaux A, Declèves A-E, Caron N, Nonclercq D, Legrand A, Toubeau G (2010) Expression of nestin, vimentin, and NCAM by renal interstitial cells after ischemic tubular injury. J Biomed Biotechnol 2010:193259
Whitford GM (1994) Intake and metabolism of fluoride. Adv Dent Res 8:5–14
Zou J, Yaoita E, Watanabe Y, Yoshida Y, Nameta M, Li H, Qu Z, Yamamoto T (2006) Upregulation of nestin, vimentin, and desmin in rat podocytes in response to injury. Virchows Arch 448:485–492
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
All experimental procedures were done according to the National Institutes of Health (NIH) guidelines for the Care and Use of Laboratory Animals. An approval of the current protocol was obtained from the Institutional Animal Care and Use Committee, Zagazig University, Egypt (ZU-IACUC /2 /F /119 /2019).
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Mohamed M. Abdel-Daim
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Saber, T.M., Mansour, M.F., Abdelaziz, A.S. et al. Argan oil ameliorates sodium fluoride–induced renal damage via inhibiting oxidative damage, inflammation, and intermediate filament protein expression in male rats. Environ Sci Pollut Res 27, 30426–30436 (2020). https://doi.org/10.1007/s11356-020-09366-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-09366-z